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COGNITIVE SCIENCE Vol 24 (3) 2000, pp.

543–570
Copyright © 2000 Cognitive Science Society, Inc.

ISSN 0364-0213 All rights of reproduction in any form reserved.

Evolution of Primate Cognition
RICHARD W. BYRNE
University of St. Andrews

Comparative analysis of the behavior of modern primates, in conjunction with an accurate phylogenetic tree of relatedness, has the power to chart the early history of human cognitive evolution. Adaptive cognitive changes along this path occurred, it is believed, in response to various forms of complexity; to some extent, theories that relate particular challenges to cognitive adaptations can also be tested against comparative data on primate ecology and behavior. This paper explains the procedures by which data are employed, and uses the best currently available evidence to derive a proposal for some of the stages through which human cognition evolved, before the last common ancestor with a nonhuman, and the reasons that cognitive adaptations were favored in primate evolution.

I.

INTRODUCTION

The excitement for psychologists of investigating the cognition of primates derives from what it may reveal about the evolution of cognition in one specific primate, Homo sapiens. Primate data gives us direct insight into the evolution of cognitive capacities that arose before the last common ancestor we share with our closest relatives, the two species of chimpanzee; for more recent evolution, archaeology and paleontology take over, but interpretation of their data can also be informed by primate comparisons. Humans are highly specialized for intelligence, to judge by the morphological correlate of cognitive function, the brain. The human brain is about six times as large as that of a typical mammal of human body size (Jerison, 1973). Adult brain size is a consequence of both brain size at birth and postnatal brain growth. Some primates specialize in one or other of these methods, and in general there is a trade-off between them, with the extent of postnatal brain growth inversely related to relative neonatal brain size (Harvey & Clutton-Brock, 1985). Humans lie off this regression, both methods contributing to the development of a brain uniquely large for a primate, with disproportionate enlargement of association areas (Deacon, 1990). Humans suffer from this in two ways. Large brain size at birth, in conjunction with a narrowed pelvis associated with efficient modern bipedal-

Direct all correspondence to: R. W. Byrne, University of St Andrews, School of Psychology, St Andrews, Fife KY16 9JU, Scotland. E-mail: rwb@st-and.ac.uk.

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ism, has the consequence of difficulties and danger to mother and child during birth. Yet, much postnatal brain growth is still necessary to reach the adult size, so that the human infant is unusually helpless at birth and dependent for several years on time-consuming parental care. In particular, the costs of lactation to a human mother are substantially a result of brain size, since brain tissue is metabolically expensive, and for a time in early childhood the brain makes up 50% of basal metabolic rate (BMR; Armstrong, 1983; Milton, 1988). Even as an adult, the brain’s contribution to BMR falls only to 20%, the highest fraction in proportion to its size of any organ (Aiello & Dunbar, 1993). Because neural tissue is unstable, this energy supply has to be kept up remorselessly: even anoxia for a few minutes risks permanent brain damage. Evolution cannot result in net disadvantage for a species: in all cases, when “disadvantages” arise in evolution, they do so as a side effect of changes having overwhelming benefits overall. The numerous costs attendant on human cognitive specialization imply that intelligence has had major evolutionary advantages during the evolution of the species. There are several possible approaches to discovering when and how these evolutionary advantages had their effect. Archaeological and paleontological examination of the traces left by human and nonhuman primate ancestors reveals signs of behavior (Mithen, 1996). Direct fossil evidence of behavior is rare except in recent human ancestry, and even categorization of skeletal material into “species” is not straightforward (Tattersall, 1995), since interbreeding is a matter of behavioral choice, not body shape. Even for the most recent extinct hominids, the Neanderthals, estimates of the relationship to modern humans have varied frequently in recent years (Stringer & Gamble, 1993).1 Further back in time, with fossils of early hominids and apes, the problems only become more severe. While it is tempting to treat a fossil species as ancestral to whatever extant species it most resembles, the fact is that the fossil may have had no descendants, and its existence may only document one of the many lineages ending in extinction. At the opposite extreme, the “design” of any organism can give clues as to how and why it evolved (Dawkins, 1986). With this logic, the organization of the modern mind can be “reverse engineered” to deduce past evolutionary processes (Barkow, Cosmides & Tooby, 1992). Of course, the environment of most modern humans is so recent, in evolutionary terms, as to have had little impact by genetical selection; we are, in a sense, adapted to a vanished world. In taking the argument-from-design approach, human characteristics are assumed to be adapted to living as hunter/gatherers in the Pleistocene (Tooby & Cosmides, 1992), a period that lasted for millions of years. Unfortunately, knowledge of the Pleistocene period of human ancestry is itself imperfect (Foley, 1996). Worse, several of the extinct hominids whose stone tools define the period are now considered not to be closely related to modern humans (Mellars & Stringer, 1989). Knowledge of the Pleistocene is least sketchy in Europe, the Near East and Asia, where numerous bones, tools and living floors of Homo erectus, H. heidelbergensis, and H. neanderthalensis allow some fairly clear pictures of their lives to be built up, including tantalizing signs of big-game hunting with spears at 400 thousand years ago, and at more recent dates, burial and use of fire. However, the evidence from molecular systematics points to a relatively recent, African origin for all modern human populations (Mountain,

their cultural and cognitive achievements parallel but may not have affected those of Homo sapiens. so it is convenient to discuss the two separately. and H. and outline the current range of theories that they support. Fortunately. comparative primate analyses inform the data of archaeology and palaeontology (Mithen. we may inquire about the historical aspects: at what approximate date did the characteristic first evolve in the lineage under consideration. in what ancestral species. In this case. monkeys. and even nonprimates. 1996). Each contribution may be understood as an answer to the same question. say. the process of evolution is not subject to direct experimental testing. based on co-operative hunting of big-game. some of the most convincing accounts given of the likely evolutionary origins of modern human traits—patterns of infanticide and homicide (Daly & Wilson. 1996). heidelbergensis. Because there is no doubt that each living species shares a common ancestor with humans at some point in the past. 1990. In reality. H. All of these questions may be addressed without touching on the second contribution. II. In the first place. and (for more ancient characteristics) other species of animal. H.EVOLUTION OF PRIMATE COGNITION 545 1998). only side-branches of a “bushy” tree of hominid evolution. 1992)—are based on design principles that apply to apes. important human traits have a much greater antiquity than the Pleistocene. because behavior as well as form can be studied. and manipulated in experiments in the wild and in captivity. the causative aspects: what environmental features so significantly favored the new characteristic that natural selection perpetuated it in subsequent generations. erectus. the species distribution of a characteristic contains evidence about its origins in the human lineage.” but neither provides a complete answer on its own. for any characteristic except those that evolved solely in the last few million years of human ancestry. 1995b). This paper will attempt to explain how these data can be read. Only from the last 40 thousand years is there any evidence that direct human ancestors pursued a lifestyle close to that of modern hunter/gatherers. Already. not specifically to Pleistocene hunter/gatherers. use of fire. This period is not orders of magnitude greater than. so the logic of “adaptation to the Pleistocene” is compromised. APPROACH To describe “the evolution” of any characteristic. 1989. and before or after which other characteristics. Animal behavior is available to be observed systematically. What both share is that the evidence we have available is necessarily of an indirect nature. in most cases within essentially the environment in which it evolved. (This . partner choice and matrimonial systems (Buss. morphological or behavioral. Wilson & Daly. the 8 thousand years of Neolithic agriculture.2 and out of what original set of genetically encoded characters was it selected. the evidence for each is of a different kind. Although in reality the causative and historical aspects are intimately and logically related. requires at least two contributions. there is an additional source of evidence available: the nonhuman primates. Clearly. home-bases and living-shelters. “How did the characteristic evolve?. This comparative evidence is particularly valuable for understanding the evolution of cognition (Byrne. neanderthalensis would then be seen as derived from a much earlier “Out of Africa” spread.

on the basis of possession of shared. III. like the vertebral column. THE EVOLUTIONARY HISTORY OF PRIMATE COGNITION Methodology for Inferring History Establishing a reliable pattern of descent. in which species share characters by independent evolution in separate lineages (such as the large bodies of both elephant and hippopotamus. The evidence itself is certainly imperfect. there is inherently less certainty about the larger phylogenetic groupings: the precise delineation of the grouping “animals” is harder to establish than that of the grouping “Old World monkeys.”) It is crucial for this grouping process to distinguish derived from primitive characteristics. because the shared characters that distinguish its members from humans (small brain. The grouping of “nonhuman great apes.) are all primitive characters. 1986).) For these reasons. (Note that. rather than simple adaptations with obvious utility. The diagram produced by recursively grouping clades together is called a cladogram. this is particularly the case with DNA. Reconstructing evolutionary history from the evidence of extant species depends on a reliable evolutionary phylogeny (Ridley. in this example.” formerly called Pongids. in which species are put together into valid phylogenetic groupings. by genetically coded traits that arose in the common ancestor of the clade. unrelated species formerly grouped together as Pachyderms). However. Convergent evolution. (The proper clade here includes humans as well as nonhuman great apes. derived features. In such a taxonomy. thus there was no common ancestor of nonhuman great apes that was not also a human ancestor. and indeed monkeys are smallerbrained and hairier than humans. called clades. monkeys form an appropriate out-group. The traditional remedy has been to rely on complex and inherently unlikely structures. retentions from earlier species. is not a valid phylogenetic grouping. 1993). but the important point is that the process of relating evidence to theory will remain the same. the difficulties are exacerbated by the fact that cognitive mechanisms themselves are knowable only indirectly. species are grouped together in a way that reflects the relative recency of their divergence in the branching process of evolution. 1966). has long been known to form a potential pitfall in this process. some definitely less closely related species. and refinements in data collection may result in changes to conclusions. since “higher” groupings in the cladogram are based on fewer shared. etc. not merely to those about cognition. from the organization of observed behavior.) Primitive characters are usually identified by comparison with an out-group. hairiness. the discovery that portions of the immensely complex biological molecules are relatively inert structures not much subject to active selection has made classification by molecular similarity attractive to taxonomists (see Ridley.546 BYRNE applies to all evolutionary claims. like wings. in this paper I will endeavor to make explicit the processes by which evidence has been used to deduce the evolutionary stages in primate cognition and their causes. This is best derived by cladistic analysis (Hennig. derived characteristics— that is. in which large sections of the . However.

based on the calibration of setting orangutan/human to 12 Ma. pers. and DNA sequencing is now the preferred technique. Ko ¨ hler. Martin & Pilbeam. humans are a much closer relative than the Asian orangutan. From the point of view of a chimpanzee or a bonobo. 1994.EVOLUTION OF PRIMATE COGNITION 547 Figure 1.. The numbers at some branch points are the approximate estimated dates of divergence. Cladistic analysis using DNA sequence data has amply confirmed the dramatic result of earlier. molecule have no phenotypic expression at all. comm. 1996): chimpanzees are more closely related to humans than they . simpler methods of molecular classification: humans are far closer related to some nonhuman primates than was formerly thought (Jones. in millions of years. but this seems overly conservative since no possible orangutan ancestors are known that early (M. Only those genera mentioned in the text as contributing evidence of cognition are included. but most modern evidence strongly supports the chimpanzee-human clade (Goodman et al. a date of 16 Ma is used for this. which can be justified by the existence of Dryopithecine ape fossils at that date that show some derived characters of the orangutan. and the main higher level groupings about which reliable deductions can be made are labeled.). The exact resolution of the relationships among the African apes has been controversial. More often. Primate phylogeny. 1992). Kim & Takenaka. humans now appear deeply embedded within the African great ape clade (Figure 1). Instead of occupying an entirely separate clade to the apes.

independently in many lines of descent. would be highly unparsimonious. deduced ancestor. 1967. 1995b). and in clades defined by only a few species uncertainty is introduced if there is any variation in characteristics.. we again examine the morphological and behavioral characteristics of its descendants.) However. in this case all characteristics are relevant. Suwa & Asfaw. an early hominid from 4.4 million years ago has recently been found that possessed shared. but calibration of the clock also depends on an accurate date for at least one ancestor species (i. for a branch point in the cladogram). Furthermore. and can thus be studied by comparative analysis. The idea in that enterprise is that. Evolutionary reconstruction should be sharply distinguished from the use of living species as “models” of past phases in the evolution of other species. the robustness of this method in the face of species variation depends on the number of living species that can be examined. However. but lacked specific characters of the gorilla (White.548 BYRNE are even to gorillas. To work out what such a species was like. Nevertheless. identifying a fossil species as ancestral to a living one is hard. 1996). so that it is least straightforward to establish that part of the history of primate cognition of greatest interest for psychology. not an adaptive product of natural selection. not just the shared. There are between two and three hundred species of primates. encourages the possibility that significant aspects of human cognition evolved before the split. This relatively small span of human evolution. while evidently each living species has evolved for just as long as any other since their lines of descent originally diverged. in particular of humans. it is possible that all significant evolutionary changes might have been on one line rather than the other. recent attempts to do so have agreed with the earliest molecular taxonomy. Inferring characteristics of extinct ancestors. The concept of a “molecular clock” depends on assuming that mutation rates have not changed significantly in recent geological time. the process of using it to infer evolutionary history is a rather different one. suggesting that the real divergence time was nearer 4 than 6 million years ago. Once a reliable phylogeny has been established. derived ones. and that most mutations are neutral. . (To suggest that evolution repeatedly converged on the same character. since divergence from the lines leading to other primates. Both these assumptions are likely to be realistic (and unexpressed portions of DNA may be chosen to ensure an absence of active selection). Each inferred species is definitely ancestral to all the living species in the clade that defines it. Each branch point in the cladogram identifies an extinct species that lived at and perhaps before the date given by a calibrated molecular clock. For reasons already mentioned. whether or not any fossil is ever found that might match it. but most are monkeys and relatively few great apes survive. and finding the precise ancestor that corresponds to an identifiable branching point on a cladogram is harder still. which might be called evolutionary reconstruction (Byrne. in estimating a likely date of only 4 – 6 million years ago for the last common ancestor we share with the two species of chimpanzee (Sarich & Wilson. Characters found in all or most of the living descendants can be safely assumed to be derived from the extinct. Translating these relationships into estimates of likely dates for the divergence times is more problematic. Waddell & Penny. 1994). derived characters of chimpanzees and humans.e.

Even to make these pronouncements about the historical development of cognition in three of the populations ancestral to modern humans. Those of greatest interest for cognition are species on the human lineage. the monkeys and apes. of all great apes. including the ancestors of all primates. such as in the deep ocean. the earliest primates were not cognitively distinguished from most other mammals. Because linguistic communication requires participants to model the mental states of interlocutors. This adaptation was established before 12 Ma. Perhaps a living fossil of some early stage in primate and human evolution may exist—the tarsier is one candidate— but only evolutionary reconstruction of the ancestor concerned will allow us to identify any living fossil as such. or a purely cognitive reorganization not much related to brain size. understanding mental states was a crucial precursor to the development of language at some point in the hominid branch of the ape lineage. actions and events. some time before 30 Ma (millions of years ago). and wildly improbable that a whole series of species should have done. of Old World monkeys and apes. “monkey” (usually a macaque). including humans. it is now clear which ancestral species can in principle be reconstructed. developed the ability to understand the causal connections between objects. the simian ancestor. the coelacanth Latimeria. In contrast. an adaptation that required substantially larger brain size in relation to body size. a discredited approach still retailed sadly often in the media. The evolutionary path of cognition. it is inherently less likely that any primate species should have remained essentially unchanged for millions of years. This ancestral population gave rise to all modern simians. when the series “prosimian” (usually ring-tailed lemur). is to rely on data that are not universally accepted—for instance. since possession of language greatly increases the efficiency and sophistication of mental representation. and of specifically the chimpanzees and human. however. . with only one unusual genus. which primate is capable of which particular feat. At present there is adequate evidence to make generalizations only about the cognition of three of these species: the primate ancestor. Unfortunately. Stasis of this kind is rare. that the representational ability of the great ape ancestors was nowhere near as elaborate as our own. one species would be in effect a “living fossil” of the other. and some bottom-living sharks are good examples of living fossils of very ancient forms. Modern Nautilus. of African great apes. and most likely when the environment is unusually constant. this is more likely to be based on a misunderstanding of evolution as progressive. It is likely. the mental states of other individuals. of all simians (the shared ancestor of tarsiers and simians will be difficult to reconstruct. Then. one branch of the simian lineage. “ape” (usually the chimpanzee) and human is used to illuminate evolution. Subsequently. but it is not clear whether it depended on an increase in absolute brain size.EVOLUTION OF PRIMATE COGNITION 549 In this case. of all apes. and the great ape ancestor (see Figure 2). and the hierarchical organization of behavior. on one of the two branches). Thanks to the revolution in taxonomic techniques. Tarsier. On current evidence. plus the ready availability of those three species in the laboratory. ancestral specifically to modern great apes and ourselves. one branch of their descendants became specialized for more rapid learning.

the few species examined have proved . Hypothetical evolutionary path of primate cognition. nor any convincing evidence of tactical deception (Byrne & Whiten. independent replication of results. 1990b). they do not show the differentiation of reaction to different individuals known from monkeys (Cheney & Seyfarth. Current Evidence of Primate Cognition The primate ancestors. 1897). In laboratory testing. In order to indicate how the picture I have sketched was actually derived.) Note that it is not likely that any of the surviving species are “living fossils” of extinct forms deduced from phylogeny.550 BYRNE Figure 2. the next section will give a terse overview of the evidence as it stands at present. and which details may need modification. (See text for explanation. 1992). Thus the population ancestral to all living primates was not likely to have been specialized for intelligence. 1981). The brains of strepsirhine primates (lemurs and lorises) are no larger in relation to their body mass than those of most other mammalian orders (Passingham. which of the behavioral data are already robust. and to fill in other gaps in the evolutionary sequence. 1992). However. and even the extinct giant lemurs of Madagascar were very small brained (Forsyth-Major. improvements in methods. Most strepsirhines are small animals so that their brains are also small in absolute terms. Although some lemurs are group-living. This deduction from morphology is supported by what is currently known of the behavior of strepsirhines. nor evidence of the use of third-parties in attainment of goals or social dominance (Harcourt & deWaal. and extension to a greater range of species can be expected to increase the robustness of the somewhat tentative claims made here.

In these species. However. de Waal & van Roosmalen. 1997c. Seyfarth & Cheney. 1997). living in semipermanent groups in which social sophistication was important to survival. 1990a. importantly. but not to show any qualitative difference in cognition from them. Furthermore. that is. 1984). ancestral to all modern monkeys and apes. this sophistication may have been based only on rapid learning. Various social manipulations have been described. the social sophistication of some large Old World species. because grooming takes time it is an honest indication of the importance of the groomee to the groomer. 1997. unlike other mammals tested (Tomasello & Call. 1981). When key relationships are put at risk by conflict. simians (monkey and apes) have brains averaging twice the size of a typical mammal of their body mass (Passingham. although the lack of systematic knowledge makes any conclusion difficult. was unexpected. 1990). and dyads that reconcile are more likely to continue to support each other (Cords. not different from most other mammals. but in fact when the data from monkeys were examined. rank is strongly a function of social manipulation and support (Chapais. 1991). Even so. 1979). 1983b). such as oddity or same-different. monkeys learn tasks rapidly compared to most mammals tested (Passingham. rather than any elaborate mental representations. the conservative assumption is that the cognition of the earliest primates was primitive. and not particularly distinguished in other aspects of cognition (Tomasello & Call. 1988. Direct tests of monkeys’ understanding of other individuals’ mental states have proved negative (Cheney & Seyfarth. 1964). Datta. The simian ancestors. 1985. Building up differentiated relationships with many individuals. Given this picture. Byrne & Whiten. In contrast to strepsirhines. Old World species. were thus likely to have been relatively large-brained animals. 1990). Parks & Novak. does require good memory. 1992. not simply the larger. 1982). it does not seem to require more. Tactical deception might in principle give evidence of understanding other minds. it was concluded that all could be accounted for by very rapid learning. 1997). revealed in the research of the last 20 years. Povinelli. Strum. so the absence in New World monkeys of any use of grooming to build up social support may not reflect any cognitive inferiority. 1983). and are able to learn category discriminations that depend on comparisons of objects. not only by kin but also by “friends” (Smuts. including keeping a tally of grooming received and whether past help was returned in reciprocated support. capitalizing on the reinforcement of fortuitously beneficial— but accidental—actions (Byrne. the ability of monkeys to show real understanding of either the physical world or the mental world of their companions appears highly limited. The earliest simians. so that the brains of the larger species are also large in absolute terms (Martin. One prediction to follow . individuals make efforts to reconcile. some very subtle (de Waal. In laboratory testing. Supportive relationships are built up by means of social grooming (Dunbar. All monkey groups show deception. but only tactical deception has been evaluated over a wide range of species (Byrne & Whiten. Early simians were thus likely to have been quantitatively superior to most other mammals. 1981). To the extent that it has been studied. 1992). many monkeys and all apes are quite large animals.EVOLUTION OF PRIMATE COGNITION 551 much slower at learning than monkeys (Jolly.

and in this domain too give some evidence of real understanding.. found in great apes but not in monkeys (Gallup. but great apes show a flexibility in gestural communication that appears lacking in monkeys: development of the use of novel communicative gestures has been seen in both chimpanzees and gorillas (Tanner & Byrne. 1991. there are signs of greater understanding of social moves. having some sort of “theory of mind” about the deceptive intentions and malleable beliefs of other individuals. able to use sophisticated physical skills and social tactics— but only skills and tactics that can be learnt without an understanding of how they work. some of the records from great apes could not. Several of the data initially claimed to show that apes (but not monkeys tested in the same way) can represent the intentions of others have been reinterpreted in other ways. but it remains possible that these forms of “functional teaching” may not rely on the mothers’ understanding their infants’ knowledge base. but none is yet universally agreed. certainly shows that apes have superior cross-modal . Fouts. in great apes. 1995. In most cases. Garett & Oser. but rather responding on the basis of a genetical adaptation. Kralik. The great ape ancestors. but see Hauser. great apes show more sophisticated interactions with the physical environment than monkeys. Nagell. Furthermore. 1970. 1989). individuals of all four great ape species have been taught gestural or ideographic “languages” with some success (see especially Savage-Rumbaugh et al. 1996. Deliberate instructional teaching has occasionally been reported in chimpanzees (Boesch. Tomasello. 1994. Mitchell & Boccia. 1992). 1994). without gross distortion of the meaning of “plausible” (Byrne & Whiten. 1996). The ability to recognize one’s face in a mirror. and cheetah mothers encourage their infants’ hunting and killing skills (Caro. the evidence has first seemed to imply that only one species was capable of a feat. often with effect. usually the well-studied chimpanzee. Gust & Frost. 1991). and positive evidence has repeatedly been challenged. whereas all observations of tactical deception in monkeys could be plausibly explained as a result of very rapid learning. The idea that any nonhuman might possess a theory of mind is a strong claim. Botto.3 Also.552 BYRNE from this is the that relatively large-brained species within other orders of mammals should similarly prove quick at learning. Parker. For instance. and then to the less tractable gorilla. Olguin & Carpenter. Tomasello. Many of the data on social sophistication are clearer in some well-studied monkeys than in any great ape. differences emerge not in what great apes do—which is in practice often much the same as what monkeys do— but in how they do it. but not in any of the equally well-studied monkey species (Caro & Hauser. but not monkeys. Fouts & Van Cantford. 1994. 1989). In terms of what is seen. there has been considerable effort devoted to devising a conclusive laboratory test. 1995). Call. Monkey mothers do regularly encourage their infants’ locomotion (Maestripieri. Deception data points to great apes. However. 1993). but it is likely that great apes are similarly able to deploy social tactics and skills. This has yet to be attempted with any monkey. It remains unclear what species differences in cognition among nonhuman great apes are real ones. but later work has extended this—first to the orangutan and bonobo.

and many tool types have now been described (McGrew. and the manufacture of stone tools has been induced in orangutans and bonobos (Toth. 1993. In the wild. chimpanzees demonstrate that they possess a mental specification of an appropriate tool when they . 1992). The test individual can clearly see whether or not this is the case. if tasks can potentially be learnt over time without mentalistic understanding. 1990a). or in a position where its view is obscured. Sevcik & Rumbaugh. giving just as many alarm calls in both cases (Cheney & Seyfarth. Nelson & Boysen.EVOLUTION OF PRIMATE COGNITION 553 transfer. Similarly. A box containing food is deliberately marked by an experimenter placing a token on top of it (Call & Tomasello. The decline is presumably a response to the oddity of constant “accidents” by the experimenter. since they remove the fastlearning problem. a test animal without any ability to attribute mental states could come to link the communicative signs associated with deliberate marking with gaining a reward. Another approach centers on the perception of accidental actions. while in each such experiment the case for theory of mind is thereby rendered “not proven. However. compared with macaque monkeys that need to learn the new role from scratch (Povinelli. The chimpanzee and the orangutan (van Schaik. only later increasing to a moderately high level again. however. Fox & Sitompul. Savage-Rumbaugh. 1992). over many trials. only the intrinsic improbability and importance of nonhuman theory of mind argues for extreme stringency. intentional acts. and discriminate those cases from ones where the person acts as if making and correcting an accident. Other tasks more clearly test mental state understanding. in preparation). 1972). Wright. Conditions differ according to whether the other animal is also able to see the threat. in fact neither chimpanzees nor orangutans did increase their discrimination over time. 1989). In one. but many ape/monkey differences are vulnerable to interpretation as differences in learning speed. 1993). the chimpanzee’s facility in taking over an untaught role in a two-person cooperative task. However. (It must be noted that.” the data are often more consistent with this interpretation. the most convenient “predator risk” is a veterinarian in white coat!). all great apes commonly use and make tools (McGrew. In captivity. An ape/monkey difference in cognitive approach may also exist in the way in which they can exploit the physical world. sharply differentiate. and later “notices the mistake” and with some irritation removes the token. without invoking theory of mind (Heyes. 1996) are the only primate species regularly to manufacture and use tools for subsistence in the wild. 1998). may be explained as a superior understanding of cause and effect in great apes. an individual sees an imminent risk to a close friend or relative (in the laboratory. Chimpanzees. the same pattern was shown by people when similarly tested. the experimenter also “accidentally” knocks a token onto another (empty) box. Clearly. but the exact reverse: their accuracy was highest on trial one and then declined. Chimpanzees seem able to distinguish between knowledge and ignorance in other individuals. yet macaque monkeys apparently make no distinction. the two boxes remain marked for exactly similar periods of time. Schick. but perhaps not an ability to understand mental states (Mitchell.) Some recent tasks offer hope of an agreed resolution. Chimpanzees and orangutans seem able to discriminate accidents from deliberate. 1993). making alarm calls only when they can see their friend is unable to see the threat (Boysen.

1994). Tomasello. 1990. but so too do the plant processing techniques of mountain gorillas (Byrne & Byrne. There is now increasing evidence that great apes can copy novel human actions (Custance. and those that had learnt to use a stick to push a peanut from a tube. rather than the employment of an object as a tool. population consistency in overall technique. Might great apes have more efficient mechanisms with which to acquire novel skills? Monkeys apparently have great difficulty in imitating the actions of others (Galef. still repeatedly tried to break the nut with blows of the thin twig or used stones to extract kernels. At first. 1986). Westergaard & Fragaszy. the difference observed in the wild may derive from social learning mechanisms. when the stick was removed would attempt to get the nut by pushing short sticks in both ends of the tube. 1987). capuchin monkeys will readily learn tool use.554 BYRNE select suitable objects well in advance of the anticipated use as a tool (Boesch & Boesch. or try to probe with chain or a stick to thick to enter the tube. No such errors have been reported in many years of observation of chimpanzee tool-use under natural conditions (Goodall. 1998): the logical organization. Whiten & Bard. and its function may be a largely social one (Meltzoff & Gopnik. per se. combined with great idiosyncratic . Byrne & Russon argue that all great apes show this sort of imitation. It would seem that both monkeys and apes are sensitive to the properties that affect how tools work. 1994. or deliberately prepare a tool before carrying it to the site of use (Goodall. This raises the possibility of a monkey/ape difference in the complexity of behavioral organization that can be learnt without human intervention. and experiments on how they did so suggested deficient understanding (Visalberghi & Limongelli. 1987. No monkeys regularly make or use tools in the wild. Russon & Galdikas. Instead. Anderson & Henneman. 1996. Visalberghi & Fragaszy. show an appreciation of which dimensions are relevant to tool function when they choose among proffered objects (Hauser. Visalberghi & Trinca. more recent studies with capuchins have found them able to select and modify sticks according to the necessary properties of an efficient tool (Anderson. SavageRumbaugh & Kruger. which do not normally use tools even in captivity. complex skills by observation. 1993. imitation would be needed at a higher level in the hierarchical structure of behavior. 1996). this sort of “action-level” imitation would be of little use for learning complex skills. 1991). 1994. However. 1986). and the key aspect of great ape tool-use may be the complexity of their actions. Tanner & Byrne. based on several different sorts of evidence: in the case of mountain gorillas. In captivity. To learn novel. bimanual co-ordination and subroutine structure. it appeared that the difference lay in the ability to represent the cause and effect relations between tool and task. 1996. 1993). Chimpanzee tool use traditions show elaborate structural organization (McGrew. 1988. including the sequence of actions. although nonhuman great apes lack the very prominent copying of social actions that even very young children show (Meltzoff. 1997). 1996. and the extent to which great apes copy arbitrary actions may be influenced by exposure to humans (Call & Tomasello. 1992). 1992). 1993). On the other hand. Capuchins that had learnt to break nuts with stones and use twigs to extract the kernel. the “program-level” (Byrne. Whiten & Ham. Even tamarin monkeys. 1988). Byrne & Russon. 1995. 1984).

1979). the cognitive difference may reflect an emergent property of absolute size. once evolved. The underlying cognitive superiority of great apes over monkeys is not easy to pinpoint. even obvious. or an organizational change in “software” unrelated to volume. to come to serve an entirely different function (Gould. it becomes less surprising that there exist no compelling field observations of “before/after” differences that show imitation after a single observation of a skilled model. able to undertake simple planning and to use others’ behavior as a source of knowledge. If repetition is essential for imitation of this kind (as argued by Russon & Galdikas. but highly modular. in the case of orangutans. but there is no current evidence that they can acquire complex novel behavior by observation. but becomes more likely with adaptations of very general usefulness. 1998). their brains are of greater mass than those of any other primates. 1995). 1993). interpopulation differences in tool-using tradition that cannot be explained by ecology (McGrew. attempting to discover them. based on the model of complex food processing. but that this imitation depends on repeated observations over trials (Whiten. 1996). cognitive mechanisms of very general utility will tend to lack distinctive cues in design. In relation to body size. 1997b). has found that chimpanzees do tend to copy a demonstrated sequence of actions. 1989. The selective pressures that gave rise to primate cognition operated in the distant past. THE EVOLUTIONARY CAUSES OF PRIMATE COGNITION Methodology of Inferring Function in Cognitive Evolution Exaptation and modularity. Monkeys may prove to be able to represent cause and effect relations among objects. If so. 1981). consisting of a set of encapsulated “Darwinian algorithms” serving specific functions (Cosmides. nor comprehend the intentions that lie behind such behavior. copying elaborate human traditions of skilled action (Russon. in the case of chimpanzees. are thus potentially subject to exaptation. it is possible for a trait. but perhaps it can best be described as an ability to form and manipulate representations of instrumental behavior and mental states (Byrne. indeed. These presumed problems are a consequence of the general-purpose nature of cognition. Recent experimentation. Tutin & Baldwin. Unfortunately. Fodor. the . great ape brains are no more enlarged on average than those of monkeys (Passingham. this is the only plausible mechanism for the origin of any adaptations that would fail in partial form to achieve their current function. Thus the great ape ancestor would have had a cognitive system qualitatively more like that of humans. and especially any based on computation.) This so-called “exaptation” is relatively rare. deducing the evolutionary cause of a module’s existence should be more straightforward. 1979. 1983).EVOLUTION OF PRIMATE COGNITION 555 variation at the level of detail (Byrne & Byrne. IV. and yet it has recently been strongly argued that cognition is not in fact general-purpose. However. but because all species are large. we can only observe the design of the resulting adaptations and what functions they have in modern populations. Cognitive functions. 1995b. an ability that would help enable program-level imitation. Thus. such as wings too small to fly with. In addition.

One problem is to decide the best unit of comparison: perhaps closely related species are alike. Note that most of the theories were originally proposed to explain increased “intelligence. the usual approach is to assume that current function is a good clue to phylogenetic origin. evolutionary causes) remains a serious problem.e. fully resolved into a dichotomous branching cladogram. and it seems safer to leave the issue of modularity to empirical enquiry (e. Of course. Nonhuman primates can be studied in the field. 1993) rather than assuming that cognitive mechanisms are immune from recruitment to other functions.g. conclusions must remain speculative. N-1 contrasts can be obtained. memory for objects and events that have intricate constellations of features. In primate work..” and this vagueness can only sometimes be refined to specific . but a much better method is now available that uses all the available evidence. (If there are N species. but only one function is likely to be critical for driving costly evolutionary change at a given time: if the cognitive capacity of an individual were imagined to increase. and compare across species for how a cognitive trait (often as coarsely measured as “brain size”) varies with task complexity in different domains or with different measures of complexity. thought processes for solving complex problems and planning in confusing environments.. analyzing at the genus rather than species level (Clutton-Brock & Harvey. contrast analysis (Harvey & Pagel. the testing of theories about the selective pressures for cognition (i. so treating current function as indicative of phylogenetic origin is a powerful method. in which the complexity may relate to social interactions but the immediate function is to solve physical problems. This distinction is blurred by the case of social learning. Karmiloff-Smith. merely by recent common descent. divergence points on the cladogram are taken as the units of analysis: the various measures to be correlated are summed for each of the two branches and compared. and selection will be driven by this function. and I shall treat this separately. Here. a conservative approach was taken. in environments that probably differ little from those in which adaptation occurred. a cognitive mechanism may be used for many purposes. selective attention that directs processing and response onto essential aspects of a complex situation. Theories vary in the domain and nature of the complexity that is hypothesized to have been crucial in favoring cognitive advance. this cannot solve the problem of few species: if there are few contrasts.556 BYRNE degree to which the ancient algorithms postulated for humans work smoothly in the modern world casts doubt on the basic assumption. and should be lumped as “one” in analyses? In the past. there must always come a point at which only one function benefits from further increase. Exaptation of intelligence does appear routine for at least modern humans.) However. and these “contrasts” then constitute independent measures of whether the measures go together in evolution. 1980). learning to acquire elaborate skills. The selective pressures hypothesized to have favored cognition are usually categorized according to whether complexity in the physical or the social environment is crucial. All such theories propose that aspects of cognition arose for dealing efficiently with complexity: perception of structure in a confusing array. 1991). In consequence. Relating cognitive capacity to natural function.

set up the circumstances that selected for further increases in intellect and dexterity. bipedalism appeared to apply among mammals only to the hominid line. At the time this was proposed. so that a special-purpose morphological adaptation. in a primate that was already large-brained and manually dextrous enough to make and use tools. apparently using its long arms to reach up into vegetation (Ko ¨ hler & Moya-Sola. Clearly. and subsequent attempts to find a correlation between increases in brain volume and tool sophistication among hominids have been disappointing (Wynn. whereas in the closely related gorilla a need to extract plant food was year round. better visuospatial imagery. Testing the rather simpler idea. but put most succinctly and clearly by Oakley (1949). The earliest suggestion of a selective pressure for intelligence must be the venerable idea of “man the tool-maker. before their role (if any) in the historical sequence of Figure 2 can be discerned. was instead selected.” dating back at least to Franklin. an extinct European ape of 8 Ma. even now. Because this extractive foraging was seasonal. like chimpanzees. tool making could be enhanced by better manual control. might be seen as special pleading. an ability to recruit tools to the task was favored. Furthermore. whether tool-use is important to a species is a function of ecology. that extractive foraging per se selects for intelligence. so the hypothesis might not be expected to apply at that stage. (plant) tool use is found in some modern orangutans. This provides an interesting sidelight on the centrality of bipedalism. has recently been discovered to be bipedal. 1979).EVOLUTION OF PRIMATE COGNITION 557 aspects of cognition. a theory put forward to explain all intellectual advance may prove valuable in understanding one discrete stage in human and primate ancestry. reliant on tool use for extracting key resources at certain times of year. However. Parker and Gibson’s hypothesis was that the great ape ancestors were. related to the orangutan. the various approaches must first be evaluated. Their descendants would possess larger brains and greater dexterity (with bipedal gait. hand anatomy need no longer be a compromise between manipulation and locomotion). since Oreopithecus was particularly small-brained. The bipedalism of the earliest hominids. however. or better understanding of the properties of rocks under percussion. so the hypothesis is not completely disproved. Dunbar (1995) found no correlation among primate species between brain size and use of . What aspect of “intelligence” is entailed on this hypothesis is unspecified. differed from our own in that many arboreal adaptations were retained. 1988). For these reasons. and the same logic would apply. He proposed that bipedalism. but tool use has also been proposed to account for superiority of all great apes over monkeys in representation of object relationships (Parker & Gibson. they argued. so to suppose Oreopithecus was not a tool user just because no evidence of (stone) tool use has been found. Explanations that depend on bipedalism can only apply to humans among the living primates. body size and strength. because individuals making better tools would be favored. Selection pressures from the Physical Environment Tool making. 1997). such as Australopithecus afarensis. Oreopithecus bambolii. thus setting up positive feedback loops that could in principle cause spiraling increase until brain size and manual control were limited in some way.

1994. because any species that sometimes forages extractively without using tools (and there are many among nonprimate species) can be dismissed as it evidently has appropriate anatomy without a need of tools.) Spatial knowledge. and the animals’ apparent excellent knowledge of them (Mackinnon. thus. 1991. hunting of large. when at present all species except for Homo appear rather similar intellectually. Schaller. with brain size relative to body size (Clutton-Brock & Harvey. Frugivorous primates would benefit from knowing the locations and fruiting of many different individuals of many species of tree. because large brains are so costly. it is argued. The idea is that if a species is adapted to forage on diet items that are sparsely and patchily distributed. this theory can explain the generally smaller brains of strepsirhine primates. both rather large-brained species. the correlation with brain size was positive. because their morphology is strongly biased towards folivory compared to simians of the same size even in species that preferentially eat fruit or insects. Relative brain size is a good indication of the strength of the selection pressure promoting intelligence. 1963). Additional problems are the fact that gorillas do not in fact rely on brute strength for their extractive foraging (Byrne & Byrne. and any nonape that relies on tool use for extractive foraging (such as the Californian sea otter) can be dismissed as specialized. This has been tested for a large number of primate species by comparing range area. (The much greater cooperation implied by effective hunting of big game has of course been suggested to underlie more advanced intelligence in Homo. active animals has only been recorded in chimpanzees. folivorous species can survive on widely available leaves. 1996). good memory is advantageous to frugivores. then any extra processing capacity that enables prediction of when and where to forage would be favored. and degree of frugivory. (Note that frugivory is also thought to underlie evolution of trichromatic color vision (Jacobs. 1980). on the basis that it aids detection of fruit and assessment of ripeness. Testing the theory-as-proposed is beset with problems. brain size increase is a matter of better memory. 1978. and vary predictably with the complex seasonality of tropical forests.) With both range area and frugivory. This last is a problem for any account that depends on a behavior found only in one species of nonhuman great ape.558 BYRNE extractive foraging. . this result was found separately for simians and strepsirhines. However. the idea that brain size relative to body size is an appropriate index of cognitive capacity has been challenged (Byrne. Perhaps for this reason. but the latter lay on a different regression since their brains are smaller for a given body size. 1994). but may be a poor index of what cognitive activity the brain allows. because only the chimpanzee uses many types of tools. Milton. and the awkwardness of assuming obligate tool use in the great ape ancestor. A selection pressure that could apply to a much wider range of primates was originally suggested on the basis of anecdotal observations of the large ranges of orangutans and spider monkeys. despite the fact that this is found in only two out of five of its descendants. in rough proportion to the size of their home range. Here. the complexity involved in co-operative hunting has seldom been proposed to underlie ape intelligence: among primates. 1981). As well as accounting for the relative brain sizes among simians and among strepsirhines.

for a heavy ape. and within diurnal simians it correlates with frugivory (Barton. the environment includes also its social companions. However.” the way is open for treating other individuals as like the self. 1982). 1995). but it is unclear how the idea may be tested further. and that Barton interprets as selection on basic mechanisms of locating and selecting fruit. or to neocortex volume in proportion to the rest of the brain. (Also. the strong correlations between relative brain size. This complication will be most problematic in small-brained species. and if the primate brain is not acting as a computing machine then the fundamental premise of selection for cognitive function is violated.) Range area inevitably correlates with body size. Dunbar. However. and hence larger bodies. primary visual cortex is larger in diurnal simians. Of course. such as folivores. 1992). This is the idea that. 1995). the problem of safely clambering through a canopy of fragile vines and branches may have selected for an ability to treat the self as an objective entity. while relative size remains useful as a measure of the cost the species is currently bearing as a result of recent selection for absolute brain size. Selection Pressures from the Social Environment Machiavellian intelligence. This could explain the origin of the close correlation between mirror self-recognition and mental state attribution in great apes and children (Gallup. cutting in to the brain capacity available for underwriting intelligent behavior. an effect which makes a small contribution to overall brain size. especially frugivores (Barton. 1983). Once the self is “objectified. and this will increase with body size. and at the same time have larger guts. with knowledge and intentions (Gallup. but when residuals of range area in this regression are compared to absolute brain size. 1982. to minimize brain size. Arboreal locomotion. because gut tissue is next to brain tissue in metabolic demand (Aiello & Wheeler. accounting for all great apes’ ability to interpret their reflection as being themselves (Povinelli & Cant. one ingenious suggestion attempts to relate mental state representation directly to a physical requirement in ape ancestry. Shea. Instead of reflecting selection for good memory. More folivorous species can manage with smaller ranges. 1996). 1990. maintenance of bodily functions will also demand some brain capacity. Theories that link cognitive evolution to environmental complexity are normally couched in terms of increasing memory capacity or learning efficiency. Purvis & Harvey.EVOLUTION OF PRIMATE COGNITION 559 If the brain is an “on-board computer. less so in primates where much of the brain volume is associated with secondary motor and perceptual processing of direct relevance to intelligence. individuals that have large or complete overlap in their requirements . 1995). no correlations emerge (Barton & Purvis. For a social primate.” then like any computing machine it must be limited by the number of its components. 1991). there is an additional pressure for species that need large guts. 1994. Whiten & Byrne. Thus absolute size is the proper measure of cognitive power. thus the correlation of relative brain size and range area can emerge as a result of selection on body size rather than brain size (Deacon. range area and diet type may be artifacts of gut size.

In general. in humans and other primates (Brothers. Despite an apparent absence of any significant intellectual problems in the physical environment of some species. 1988. Perrett et al. 1988). 1977). The characteristics of individuals pose a memory challenge. 1982. although data on the social complexity of primates increase the plausibility of some form of social pressure for intelligence. the many cognitive achievements of monkeys and apes are remarkably impressive (Byrne & Whiten. and tendencies to be predictable or inconsistent. Kummer. their initiation of and pattern of support in aggression (Datta. because in all cases the benefits to the individual lie in social manipulation. 1953). 1988). giving a “ratchet” effect of any increase in reproductive success that results from one individual’s superior intelligence. including past reciprocation of help and failures to reciprocate (Packer. Seyfarth & Smuts. 1990. 1997a). but it brings with it major problems of competition. under the rubric of “Machiavellian intelligence” (Byrne & Whiten. thus sociality might lead to intelligence. with disastrous or amusing consequences. 1983). compared with the much weaker evidence of their knowledge about natural history (Cheney & Seyfarth. 1976). 1976). Strum. for instance . 1988). there is also relatively little sign of practical intelligence. 1983). Perhaps dealing efficiently with the problems posed by social companions was the principal selective pressure for primate intelligence? Various points have been used to argue that it was. compared to the more static complexity of the physical world. 1986). such as the gorilla. individuals’ value in co-operation. Primates also remember individuals’ past histories of group residence (Cheney & Seyfarth. because this will automatically increase the average intelligence of the next generation (Humphrey. These include: ● ● ● ● ● The inherent fluidity and reactivity of conspecifics poses a special challenge (Chance & Mead.560 BYRNE for resources.. most likely in reducing predation risk (van Schaik. and there is evidence that monkeys do indeed take account of kin associations and dominance relationships between third parties (Cheney. 1983a) and friendships with others (Smuts. 1966). To determine how best to do so. in no sense do they test the hypothesis. 1982). Predator/prey systems share the need to compute the changing actions of other individuals. It has even been suggested that this legacy of cognitive advance in social matters causes humans to interpret physical systems as if they were active social agents (Humphrey. but not vice versa (Jolly. but an individual’s social competitors inevitably have essentially the same intelligence as itself. Discrimination of individual identity and emotional state depends on face processing systems which have often been suggested to be cognitively complex. 1982). but geometrically if relationships between third parties are also noted (Whiten & Byrne. de Waal. 1989). they nevertheless show remarkable intelligence (Humphrey. 1976). However. 1983. which increases linearly with group size if only immediate relationships with the self are remembered. Evidently social living is ultimately beneficial to them. Several aspects of cognition have been invoked as components of Machiavellian intelligence (Byrne. In the socially unsophisticated lemurs. it is necessary to be more specific about what is involved.

and in insectivorous bats those species with stable social groups have larger neocortex ratio (Barton & Dunbar. all the indications of social complexity may rely only on rapid learning and extensive memory for individuals and their traits. 1981).EVOLUTION OF PRIMATE COGNITION 561 their reliability as a source of information (Cheney & Seyfarth. may require particularly rapid learning. and the social group size of monkeys and apes also overlap completely. Marino. so the Machiavellian intelligence hypothesis would give no explanation of great ape cognitive superiority (Byrne. 1978). However. 1994. social group size. 1990b). This effect is not restricted to primates. as a rough measure of the social “problem” an individual confronts. and a kind of social manipulation—tactical deception— that does not require understanding of mental states. this knowledge can be gained without individual experimentation. 1995a). Average group size. representational understanding of mechanism. Neocortex ratio predicts the amount of tactical deception that is reported for a primate taxon. And larger neocortex ratio seems to pay off in an interesting way: male rank is less closely related to mating success in species with larger neocortical ratio. which overlap between the taxa. however. in the mental simulation of the likely future behavior of competitors or maneuvers that could outwit them (Byrne. when amount of effort invested in field study is controlled (Byrne. both across species and across phylogenetic contrasts (Barton. but not necessarily any deep. 1973). In principle this could even involve mental state attribution or “theory of mind” (Premack & Woodruff. applying also to carnivores and dolphins. Living socially presents opportunities as well as problems. because the neocortex is responsible for most of the variation among primates (Stephan. Taking account of the presence and actions of third parties in aggressive encounters. 1997. some sort of problem-solving may also be involved. suggests that the selective pressure of social complexity may result in larger brains that allow rapid learning on the basis of elaborate social knowledge. Frahm & Baron. 1993. may also require substantial immediate memory capacity. 1998). or in co-operative prey capture (Boesch. suggesting perhaps that the gains of brute force can be undermined by strategy (Pawlowski. from coincidental conjunctions of events that happen rarely. Dunbar. but a direct relationship between brain enlargement and behavioral complexity in social circumstances has also been found. It is clear that the potential memory load needed to profit individually in a social environment is very large. 1997b). 1996). 1992). correlates with neocortex ratio in simian primates. Social solutions to environmental problems. and integration of several items in working memory at the same time (Byrne. 1996. such as deception. Thus far. 1997c): cats and dogs are able to acquire similar tactics in captivity. Group size is only an indirect measure of social complexity. but in the wild this has yet to be properly documented even in the large-brained social carnivores. The correlations between brain enlargement. because the knowledge of other individuals may be useful. by means of social . Using this information to learn social tactics. an ape/monkey difference in cognition cannot be explained by neocortical ratios. Direct testing of social hypotheses has centered on the use of neocortical ratios as an index of brain enlargement in the primate lineage. Teleki. when the necessary coincidences are more frequent. Lowen & Dunbar. 1996). In principle.

V. raises a new problem: how did the ability to mentally represent the organization of complex behavior evolve? There are at least two possible ways in which natural selection might have favored an ability to structure actions hierarchically. either because of generally small body size. or in larger species because metabolic constraints of their diet set an upper limit on brain size. but were able to fall back on a rather coarse plant diet. Great apes clearly must have some competitive advantage. or since. This need is sharpened by competition from Old World monkeys. and have yet to be tested systematically. enabling access to physically defended plants and insects unavailable to monkeys. Their brain sizes were relatively small. Cognitively. and is apparently absent in monkeys and strepsirhines. Nevertheless. and the long periods of dependency of monkeys and especially apes have been seen as potential “apprenticeships” enabling acquisition of skills for dealing with physical problems (Bruner. 1997b). largely insectivorous. 1996). these primates differed little from most other mammals existing at that time. . Parker. species which occur throughout the geographical range of great apes and are able to eat fruits when less ripe and leaves when tougher. Social enhancement of learning is well known in many species (Galef. I will suggest a possible scenario. nocturnal animals. This is put forward in the spirit of offering an edifice on which to hang current data. the need to process foods with greater efficiency. 1988. rather elaborate constructions of living branches that enable them to sleep in a wide range of sites. Spence. than can apes. All great ape species build nests. understanding hierarchical organization and thus constructing novel plans partly by observation. Large body size and the high energetic cost of brachiation during long-range travel makes efficient feeding a priority for living great apes. 1996). 1997b). However. one which may tempt researchers to attempt its demolition—with the result that in time a more secure structure can be created. the advantage this gives in enabling them to sleep near food has been suggested to have selected for mechanical construction skill (Fruth & Hohmann. CONCLUSIONS From what has been reviewed. Those few larger species that did exist ate a wide range of plant and animal food. it should be clear that the most obvious conclusion is that. based on the methods of evolutionary reconstruction outlined in this paper. as yet. available year-round in a relatively small range. to survive at all. whereas the direct acquisition of others’ knowledge by imitation has been difficult to establish even among great apes. and thus given rise to an ability to perceive structure in the behavior of others and so learn their skills by imitation (Byrne. 1972. Alternatively. These hypotheses are recent. has been proposed to have selected directly for skilled manual learning (Byrne. and treating the tentative conclusions summarized in Figure 2 as correct. the recent evidence that suggests that great apes can imitate the “program level” of organization of complex behavior. The early primates before 50 Ma were rather small.562 BYRNE learning. no firm conclusions about the evolution of primate cognition are wise. 1937).

enabling more efficient food processing. and to manipulate them in simple planning. and thus larger home ranges. We know from fossil evidence that most ape species did in fact become extinct. relatively large-brained descendants of these early simians. but the one species that gave rise to all surviving forms—including humans—acquired an ability to understand and to perceive the hierarchical structure of behavior. Diurnal frugivory. This required a diet shift towards higher energy foods. Furthermore. necessitating enlargement of parts of neocortex involved in social information processing. though few overt differences in social behavior. The selection pressure seems likely to have been in some way a consequence of the inefficiency of apes in quadrupedal walking. This population was ancestral to modern great apes. perhaps itself a result of a diurnal lifestyle. this is a story. This pressure derived from an environment of increased social complexity in these ancestral simians. causing a great increase in the subtlety of social lives of these animals. and their more primitive relatives. albeit one that is consistent with many of the known facts about the surviving descendants of the evolutionary events known to have taken place from phylogenetic evidence. met in part by an increase in body sizes but also necessitating a relative increase in brain size as a proportion of the body. to represent cause and effect relationships. could be represented. one population of primates was subject to a strong selection pressure for greater learning abilities. The fragility of negative evidence. the ability to represent the knowledge of other individuals was an essential precursor for the evolution of true communication in one group of their descendants. the data amounts to the finding that some species have the capacity. Inevitably. The immediate benefits of these abilities were in acquiring elaborate manual skills by individual construction and social learning. selected for trichromatic color vision and a corresponding increase in primary visual cortex. or allowing nest building and hence preferential access to food. and with elaborate social knowledge. Like any evolutionary account. at some time between 25 Ma and 12 Ma. do not. in conjunction with their need to obtain a relatively high energy diet—in competition with other species. whereas their nearest relatives. one population adapted in response to a very different selection pressure. principally ripe fruit. in addition. Brain enlargement brought increased metabolic costs. as well as physical descriptions. and had some understanding of the relationship between the properties and functions of objects.EVOLUTION OF PRIMATE COGNITION 563 At some time before 30 Ma. pinpointing when in evolution capacities first evolved. they could also form concepts based on comparisons of characteristics. and distinguished by locomotor adaptations towards arboreal clambering and swinging. Group living was most likely a response to increased predation. since sources of ripe fruit are ephemeral. able to learn rapidly. The secondary consequence was that mental states. and there are three different types of problem inherent in current data: 1. including monkeys with more efficient digestive adaptations. its accuracy is entirely dependent on the data available. Whether or not as a direct result of social complexity. Among the highly social. caused by living in semipermanent groups. the hominids. However. These early simian primates were therefore highly visual animals. The key to this is the nearest relatives who do not show the ability: thus. every claim rests on individuals .

and mirror self-recognition in gorillas (Patterson & Cohn. This paper has benefited greatly from their efforts. and if confirmed would mean a major change in evolutionary interpretation. This is unremarkable in one sense. it is liable to lead to revision of several current positions. 1999). there may be surprises in store when a broader range of monkey and strepsirhine species are studied. Tamarins looked longer in precisely those conditions in which the (human) actor violated the expectations of an observer with theory of mind.. These types of negative evidence are fragile. Rather than an attempt at a final synthesis. The species which fail to show some aspect of cognition are just as important in reconstructing evolution as those “more glamorous” ones that show human traits. and an anonymous referee. However. diurnal. but mistakes which remain are my own responsibility alone.g. concerns the use of the habituation-dishabituation paradigm to present the “Sally-Ann” task to tamarin monkeys (Hauser & Santos. Michael Tomasello. the case of whether monkeys understand the properties of a tool). or that the task is less diagnostic than had been thought. because it is very much harder to obtain quality data on small.. relatively large. It will have become obvious that the wellstudied. Now that a portion of the Neanderthal genome has been reconstructed (Krings et al. and in any case the more separate branches of the primate tree are studied. although I have usually mentioned or even discussed the disagreement (e. Unrepresentative samples of species. highly arboreal species. I have unashamedly selected the data and conclusions that I believe correct. Tomorrow. which includes all genera mentioned by name in this paper). Acknowledgments: I would like to thank those who read the first draft and gave me their helpful advice: James Greeno. However. NOTES 1. Sitompul & Van Schaik. are over-represented in the data available at present (see Figure 1. semiterrestrial species of primate. a new population may be discovered that regularly shows the behavior. 1998). Steven Mithen. Whether this shows that tamarins have theory of mind. or never having been observed showing a diagnostic behavior in the wild. the more contrasts are available for testing theories of which selection pressure led to which cognitive adaptation. 1994) are illustrative cases. 2. one very recent report that runs so counter to the bulk of the evidence. 3. or a redesigned experiment may allow individuals to show the capacity which poorer designs masked: skilled tool use in orangutans (Fox. Many areas of animal cognition are controversial: in general. If it serves to energize future research that shows it to be flawed in numerous ways.564 BYRNE of some species of animal regularly failing in an experimental task. had . let alone nocturnal ones. and the great apes. known from abundant fossil material and thousands of stone tools. and a particular focus on our closest relatives is reasonable. Unresolved controversies. 1997) we can hope to discover whether the Neanderthals. it will have done its job. the account I have given of the historical sequence and causal forces that led to the cognition of the last common ancestor we share with any animal should be seen as a challenge.

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